Assessment of the Potential of the Invasive Arboreal Plant Ailanthus altissima (Simaroubaceae) as an Economically Prospective Source of Natural Pesticides

Abstract

The extensive use of pesticides may negatively affect human health. Additionally, it is one
of the main reasons for the decline of pollinators and is thus a hazard for most crops and biodiversity
as a whole. Good candidates for the replacement of pesticides with ones less toxic to humans and
pollinators are natural products (bioactive compounds extracted from plants), even though it should
be kept in mind that some of them can be toxic too. Ailanthus altissima (Mill.), swingle, known also as
tree of heaven, (Simaroubaceae) is one of the most aggressive alien invasive plants. It demonstrates
a high tolerance to various habitat conditions and a potent propagation ability. This plant has a
prominent ability to suppress the seed development of local vegetation. The aim of this review study
is to summarize the potential of this plant for use as a natural pesticide, starting with ethnobotanical
information. The essential oils extracted from A. altissima with its main components α-curcumene
α-gurjunene, γ-cadinene, α-humulene, β-caryophyllene, caryophyllene oxide, germacrene D, etc.,
have been reported to possess different activities such as insect repellent, insecticidal, and herbicidal activity. Additionally, polar extracts and particularly quassinoids, the phenolic constituents
of A. altissima leaves, are potent phytotoxins and fumigants. The basic extraction protocols are
also summarized.

Full text

Citation: Kozuharova, E.; Pasdaran,
A.; Al Tawaha, A.R.; Todorova, T.;
Naychov, Z.; Ionkova, I. Assessment
of the Potential of the Invasive
Arboreal Plant Ailanthus altissima
(Simaroubaceae) as an Economically
Prospective Source of Natural
Pesticides. Diversity 2022,14, 680.
https://doi.org/10.3390/d14080680
Academic Editor: Kevin Cianfaglione
Received: 8 July 2022
Accepted: 17 August 2022
Published: 19 August 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
diversity
Review
Assessment of the Potential of the Invasive Arboreal Plant
Ailanthus altissima (Simaroubaceae) as an Economically
Prospective Source of Natural Pesticides
Ekaterina Kozuharova 1, * , Ardalan Pasdaran 2, Abdel Rahman Al Tawaha 3, Teodora Todorova 4,
Zheko Naychov 5and Iliana Ionkova 1
1Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Sofia, 2 Dunav Str.,
1000 Sofia, Bulgaria
2Medicinal Plants Processing Research Center, Shiraz University of Medical Sciences, Shiraz 73, Iran
3Department of Biological Sciences, Al-Hussein Bin Talal University, Ma’an P.O. Box 20, Jordan
4Institute of Biodiversity and Ecosystems Research, Bulgarian Academy of Sciences, 2 Gagarin Str.,
1113 Sofia, Bulgaria
5Department of Surgery, Obstetrics and Gynecology, Faculty of Medicine, Division of Cardiac Surgery,
University Hospital Lozenetz, Sofia University St. Kliment Ohridski, 1407 Sofia, Bulgaria
*Correspondence: ina_kozuharova@yahoo.co.uk or ina@pharmfac.mu-sofia.bg
Abstract:
The extensive use of pesticides may negatively affect human health. Additionally, it is one
of the main reasons for the decline of pollinators and is thus a hazard for most crops and biodiversity
as a whole. Good candidates for the replacement of pesticides with ones less toxic to humans and
pollinators are natural products (bioactive compounds extracted from plants), even though it should
be kept in mind that some of them can be toxic too. Ailanthus altissima (Mill.), swingle, known also as
tree of heaven, (Simaroubaceae) is one of the most aggressive alien invasive plants. It demonstrates
a high tolerance to various habitat conditions and a potent propagation ability. This plant has a
prominent ability to suppress the seed development of local vegetation. The aim of this review study
is to summarize the potential of this plant for use as a natural pesticide, starting with ethnobotanical
information. The essential oils extracted from A. altissima with its main components
α
-curcumene
α
-gurjunene,
γ
-cadinene,
α
-humulene,
β
-caryophyllene, caryophyllene oxide, germacrene D, etc.,
have been reported to possess different activities such as insect repellent, insecticidal, and herbi-
cidal activity. Additionally, polar extracts and particularly quassinoids, the phenolic constituents
of A. altissima leaves, are potent phytotoxins and fumigants. The basic extraction protocols are
also summarized.
Keywords: biopesticides; essential oils; quassinoids; invasive plants’ management
1. Introduction
Pesticides are a broad group of heterogeneous chemicals. They are toxic substances
used to kill, prevent, or control pests such as insects and other animals, plants/weeds
or fungi that harm crops, ornamental plants, stock, or, humans. In addition, they are
considered to have public health benefits by increasing food productivity and decreas-
ing food-borne and vector-borne diseases/infections caused by bacteria, fungi, or other
pathogens [
1
,
2
]. All pesticides interfere with normal metabolic processes in the pest or-
ganism and are often classified according to the type of organism they are intended to
control (e.g., herbicides; insecticide; fungicide; fumigant) [
2
]. However acute, high-dose
pesticide exposures have been known for decades to cause clinically obvious and some-
times fatal poisoning. Moreover, the subclinical toxicity with a wide range of asymptomatic
effects at levels of exposure too low to produce overt signs and symptoms should not be
underestimated—they can cause cancer, cardiovascular dysfunctions, neurodegenerative
disorders, etc. [1,3–9], and children are particularly at risk [1,8,10,11].
Diversity 2022,14, 680. https://doi.org/10.3390/d14080680 https://www.mdpi.com/journal/diversity

Diversity 2022,14, 680 2 of 16
According to The Food and Agriculture Organization, “it is estimated that the value
of pollination services to global food production is worth up to USD 600 billion annu-
ally” [
12
]. However, there is a great deal of evidence for pollinators’ global decline [
13
–
27
].
One of the biggest issues besides habitat destruction, the loss of floral resources, and
emerging diseases is the negative impact of pesticides, particularly neonicotinoids, with
more than
19,000 scientific
references addressing these environmental threats [
19
,
20
,
28
–
35
].
Herbicides and fungicides such as glyphosate, metolachlor, oxadiazon, prochloraz, propi-
conazole, etc., have been found to harm pollinators [
29
,
32
,
36
–
41
]. The essential elements
of an effective pollinator conservation policy have been summarized and the approach is
holistic and based on scientific knowledge [42,43].
To reduce the harm of the pesticides in use, it is necessary to find a way to replace
them with ones less toxic to humans and pollinators. Good candidates for this are nat-
ural products—bioactive compounds obtained from plants. Of course, this should be
approached with caution. It is well known that many poisons have a vegetal origin. It is
important to discover the ones that have selective activity. This requires an approach in
two steps. The first step is finding the pesticide activity of the natural products. The second
step involves tests for safety.
Two groups of natural products deserve attention for their possible roles as biopesti-
cides. Some plant essential oils (e.g., Thymus serpyllum,Origanum majorama,
Alpinia conchigera
,
Zingiber zerumbet,Curcuma zedoaria,Achillea vermicularis, and A. teretifolia) repel insects and
have contact and fumigant insecticidal actions against specific pests [
44
–
46
]. These actions
are attributed to the compounds amphene, camphor, 1,8-cineole (eucalyptol), terpinen-4-ol,
isoborneol,
α
-humulene,
α
-pinene,
β
-pinene, and (
−
)-
α
-bisabolol [
44
,
46
–
48
]. Additionally,
essential oils are considered potential bio-herbicides, with different and selective herbicidal
mechanisms in comparison to the synthetic herbicides [
49
–
55
] as they are active against ger-
mination and early radicle growth at different levels [
55
]. The high presence of oxygenated
monoterpenes (
β
-pinene, limonene, p-cymene, carvone, carvacrol, etc.) is related to potent
phytotoxic activity [
55
] as well as to the
α
-pinene and 1,8-cineole [
47
,
51
,
56
]. In addition, the
active phenolic monoterpenoids carvacrol and thymol have been suggested as alternative
pesticides, herbicides, and insecticides [
52
]. Many studies on the various quassinoids
(isolated compounds) from different genera have revealed the promising pesticide potential
of this class of compounds [57–59].
The search for a replacement of pesticides is worth being conducted among alien
invasive plants firstly because they are inexpensive and abundant sources of bioactive
compounds, and secondly because they obviously have the phytochemical equipment to
suppress the local vegetation and resist pests. Ailanthus altissima (Mill.) Swingle, the tree of
heaven (Simaroubaceae), is a hard to control alien, aggressive, and invasive woody plant
species [
60
–
70
]. The plant is native to northern and central China and has turned into a
noxious weed in Europe, America, Australia, and other parts of the world where it has
been introduced. [
61
]. Particularly, A. altissima is considered the most invasive alien species
in Europe together with Ambrosia artemisiifolia L. and Robinia pseudacacia L. [
61
], which
negatively affects the local biodiversity [
68
,
70
]. The tree of heaven not only outcompetes
the local plants but also suppresses their seed germination and seedling development [
71
].
Additionally, it is less attacked by herbivorous insects [61,62,66].
The aim of this review study is to summarize the potential of A. altissima for use in
natural pesticides through the following methods: (1) by summarizing the ethnobotanical
data for pesticide activity reports, (2) by identifying the groups of compounds with pesticide
potential, and (3) by summarizing the extraction protocols for each of the compounds’
groups in order to further enhance the optimal extraction protocols’ designs.
2. Material and Methods
In 2019–2022, we accessed Google Scholar, Web of Science, and PubMed to identify
publications with the search strings: “Ailanthus altissima”, “ethnobotany”, “traditional”,
“quassinoids”, “essential oil(s)”, “fumigant”, “insect repellent”, “juglone index”, “phyto-

Diversity 2022,14, 680 3 of 16
toxic”, “insecticide”, “insecticidal”, “herbicide”, “herbicidal”, “fungicide”, and “antifun-
gal”. No particular restriction was considered for the search strategy, such as publication
language or publication year. The results of the search were publications primarily in the
English language, and they covered the period from 1980 to 2021. Following the PRISMA
2000 guidelines, the records were assessed for eligibility and the inappropriate ones were
excluded (namely, 160 studies were included in the review; the excluded ones were
35 studies that did not fit to the review topic and 2 that were not reliable).
We focused on the quassinoids and the essential oils for two reasons: firstly, these
groups of compounds are known for their insect repellent, fumigant, fungicidal, and
phytotoxic potential, and secondly, quassinoids are the most prevalent constituents in
genus Ailanthus [
72
–
78
]. The aggressively invasive behavior of A. altissima suggests the
promising potential of this plant for future pesticide formulations.
3. Results and Discussion
3.1. Ethnobotanical Data about Ailanthus altissima (Mill.) Swingle
Ethnobotanical information is usually focused on the medicinal properties of plants.
Therefore, information regarding the pesticide potentials of plants is valuable but scarce.
For invasive plant species, ethnobotanical records are collected in their native ranges of
distribution. The local human populations in these regions have established traditions in
the application of such plants. The bark of Ailanthus altissima (
臭椿
chou chun) was initially
recorded in Xin Xiu Ben Cao, a renowned traditional Chinese medicine monograph [
79
].
The information within this book relates that besides the many others therapeutic effects
of A. altissima, the bark of the plant was used as an insecticide [
79
]. A. altissima plant
materials were often used in ancient China against insect predators of stored grains [
80
].
The traditional use of A. altissima in Chinese medicine represents the starting point for
scientific research seeking evidence of such pharmacological activities, and in this particular
case, its potential pesticidal effects.
3.2. Chemical Constituents of Ailanthus altissima and Extraction Methods
A. altissima contains various secondary metabolites such as alkaloids, terpenoids,
flavonoids, essential oil, etc., with a wide range of pharmacological effects such as anti-
cancer, anti-inflammatory, anti-protozoal, etc. [79,81–93]. For instance, extracts of A. altissima
stems containing ailanthone possess antiplasmodial activity against Plasmodium falciparum
P. berghei [
94
,
95
]. An interesting new discovery is the antifungal effect of the alkaloid canthin-
6-one isolated from A. altissima against Fusarium oxysporum f. sp. cucumerinum [96].
Here we focus on the quassinoids and essential oils as potential biopesticides since
there is an indication that these groups of compounds have such effects [9–18].
3.3. Essential Oil of Ailanthus altissima: Composition and Extraction Overview
The qualitative and quantitative compositions of A. altissima essential oil vary con-
siderably. This variability depends on the plant populations/ecological factors, the ex-
tractable parts, the ontogenesis stage, and the drying process. The main components
are
α
-curcumene,
α
-gurjunene,
γ
-cadinene,
α
-humulene,
β
-caryophyllene, caryophyllene
oxide, germacrene D, etc. [83,97–99].
The extraction methods are summarized here. The collection of the materials for
A. altissima essential oil extraction may take place in the summer in Tunisia [
97
,
98
] or in
September in Croatia [
83
]. The extraction of essential oil is a technological challenge as our
own experience revealed (unpublished data). Basically, the essential oil of different plant
parts (roots, stems, leaves/young and old plants, flowers, and ripe fruits, all cut into small
pieces) is extracted by hydrodistillation for 3–4 h using a Clevenger-type apparatus [
83
,
98
]
or a simple laboratory Quick-fit apparatus [
97
]. The identification of the components is
performed by GC-FID and GC/MS analyses.
Additionally, the essential oil of A. altissima bark was extracted by the Soxhlet method
with anhydrous diethyl ether until the distilled liquid became colorless. The solvent was

Diversity 2022,14, 680 4 of 16
evaporated under a vacuum in a rotary evaporator and the fumigant activity was tested
against four major stored grain insects [100].
3.4. Quassinoids Extraction, Fractionation, and Isolation Overview
Quassinoids are all-chair cyclic and highly oxygenated derivatives of squalene. Bio-
genetically, they can be regarded as the degraded triterpenoids, which are isolated exclu-
sively as bitter principles from plants of the Simaroubaceae family [101].
A. altissima is rich in quassinoids (Table 1, Figure 1) and the process of the identification
of new quassinoids is still progressing [
90
]. The concentration of ailanthone, one of the
main quassinoids, may range from 6.44
µ
g/mL to 825
µ
g/mL, depending on the source
locality in China [102].
Table 1. List of isolated quassinoids from A. altissima.
Compound CAS
Registry Number Plant Material
Contents or
Obtained Amount
mg/g Dry Weight
Ref.
12-dihydroailanthone not assigned Bark 0.027 [103]
26α-tigloyloxychaparrin 75144-71-7 Root bark 0.003 [104]
36α-tigloyloxychaparrinone 69423-70-7 Seedling 0.017 [104]
411-acetylamarolide 29913-88-0 Bark, seed 0.018 [104]
512-dihydroisoailanthone n. a Bark 0.080 [103]
613,18-dehydroglaucarubinone 68703-94-6 Root bark 0.124 [104]
7Ailanthone 981-15-7 Root, seed, leaves 0.003–0.05 [103,105]
8Ailantinol A 176181-83-2 Aerial parts 0.007 [72]
9Ailantinol B 177794-39-7 Stem bark 0.002 [72]
10 Ailantinol C n. a Stem bark 0.002 [73]
11 Ailantinol D n. a Stem bark 0.0005 [73]
12 Ailantinol E n. a Root bark 0.0004 [74]
13 Ailantinol F n. a Aerial parts 0.0004 [74]
14 Ailantinol G n. a Aerial parts 0.0007 [74]
15 Ailantinol H n. a Aerial parts 0.0002 [106]
16 Altissinol A n. a Bark 0.001 [104]
17 Altissinol B n. a Bark 0.003 [104]
18 Amarolide 29913-86-8 Bark, seed 0.001 [104]
19 Chaparrinone 22611-34-3 Root bark 0.002 [104]
20 Chaparrolide 33512-38-8 Bark 0.003 [104]
21 ∆13−18-dehydroglaucarubolone n. a Seed 0.0002 [72,104]
22 Glaucarubin 1448-23-3 Stem bark 0.003 [104]
23 Glaucarubinone 1259-86-5 Seed n. a -
24 Glaucarubol 1448-22-2 Stem bark n. a -
25 Isoailanthone n. a Root bark 0.0002 [103]
26 Shinjudilactone 80180-30-9 Seed 0.003 [107]
27 Shinjuglycoside A n. a Seed 0.012 [108]
28 Shinjuglycoside B n. a Seed 0.044 [108]

Diversity 2022,14, 680 5 of 16
Table 1. Cont.
Compound CAS
Registry Number Plant Material
Contents or
Obtained Amount
mg/g Dry Weight
Ref.
29 Shinjuglycoside C n. a Seed 0.005 [108]
30 Shinjuglycoside D n. a Seed 0.002 [108]
31 Shinjuglycoside E 112667-45-5 Root bark 0.0002 [109]
32 Shinjuglycoside F 112667-46-6 Root bark 0.00005 [109]
33 Shinjulactone A 89353-91-3 Seed 0.002 [105]
34 Shinjulactone B 80648-28-8 Aerial parts 0.001–0.004 [110]
35 Shinjulactone C 82470-74-4 Root bark 0.001 [107]
36 Shinjulactone F n. a Root bark 0.003 [111]
37 Shinjulactone G n. a Root bark 0.0003 [112]
38 Shinjulactone H n. a Root bark 0.001 [112]
39 Shinjulactone I n. a Root bark 0.0002 [111]
40 Shinjulactone J n. a Root bark 0.0001 [111]
41 Shinjulactone K 94451-22-6 Root bark 0.0005 [111]
42 Shinjulactone L n. a Root bark 0.0005 [113]
43 Shinjulactone M n. a Root bark 0.0005 [114]
44 Shinjulactone N n. a Root bark 0.0002 [114]
45 Shinjulactone O n. a Root bark 0.001 [115]
46 Chuglycoside A n. a Seed (samara) 0.003 [116]
47 Chuglycoside B n. a Seed (samara) 0.014 [116]
48 Chuglycoside C n. a Seed (samara) 0.024 [116]
49 Chuglycoside D n. a Seed (samara) 0.001 [116]
50 Chuglycoside E n. a Seed (samara) 0.145 [116]
51 Chuglycoside F n. a Seed (samara) 0.002 [116]
52 Chuglycoside G n. a Seed (samara) 0.001 [116]
53 Chuglycoside H n. a Seed (samara) 0.0005 [116]
54 Chuglycoside I n. a Seed (samara) 0.032 [116]
55 Chouchunlactone A n. a Root bark 0.0001 [90]
56 Chouchunlactone B n. a Root bark 0.0003 [90]
57 Chouchunlactone C n. a Root bark 0.0007 [90]
58 Chouchunlactone D n. a Root bark 0.0002 [90]
59 Chouchunlactone E n. a Root bark 0.0002 [90]
Different extraction and isolation procedures have been developed according to the
chemical nature and class of the quassinoids. Many of the quassinoids are categorized as
non-polar or low polar compounds. However, a significant number of polar quassinoids
have been reported as well. The extraction approach is performed either using polar, semi-
polar, or non-polar solvents. The polar group of solvents includes hot methanol, hot water,
ethanol, or similar ones [
72
–
74
,
103
–
105
]. As example of a non-polar solvent that is used
is hexane [
106
,
107
]. Generally, the procedures include the solvent partitioning and solid-
phase fractionation. In most cases, during the solvent partitioning, quassinoids concentrate
in the semi-polar solvent (e.g., dichloromethane, chloroform, and ethyl acetate) [
105
,
108
].
In the solid-phase extraction and isolation methods, various stationary phases such as silica

Diversity 2022,14, 680 6 of 16
gel or/and C-18, C-8 (reverse phase) are used [
109
,
110
]. A wide range of solvent mixtures
have been used as mobile phases with varying polarities, although a rising polarity gradient
was often considered for future separation. Methanol in ethyl acetate (with an increasing
methanol percentage), methanol in chloroform, and methanol in acetone are some of the
most popular eluents [57,114].
Diversity 2022, 14, x FOR PEER REVIEW 6 of 17
Figure 1. Cont.

Diversity 2022,14, 680 7 of 16
Diversity 2022, 14, x FOR PEER REVIEW 7 of 17
Figure 1. The structure of quassinoids isolated from A. altissima. The compound numbers corre-
spond to the list in Table 1.
Different extraction and isolation procedures have been developed according to the
chemical nature and class of the quassinoids. Many of the quassinoids are categorized as
non-polar or low polar compounds. However, a significant number of polar quassinoids
have been reported as well. The extraction approach is performed either using polar, semi-
polar, or non-polar solvents. The polar group of solvents includes hot methanol, hot wa-
ter, ethanol, or similar ones [72–74,103–105]. As example of a non-polar solvent that is
used is hexane [106,107]. Generally, the procedures include the solvent partitioning and
solid-phase fractionation. In most cases, during the solvent partitioning, quassinoids con-
centrate in the semi-polar solvent (e.g., dichloromethane, chloroform, and ethyl acetate)
[105,108]. In the solid-phase extraction and isolation methods, various stationary phases
such as silica gel or/and C-18, C-8 (reverse phase) are used [109,110]. A wide range of
solvent mixtures have been used as mobile phases with varying polarities, although a ris-
ing polarity gradient was often considered for future separation. Methanol in ethyl acetate
(with an increasing methanol percentage), methanol in chloroform, and methanol in ace-
tone are some of the most popular eluents [57,114].
Many of the quassinoids could be formed as crystalline matters. Hence, quassinoids
are purifiable phytochemicals [111–113].
For the phytotoxicity and larvicidal tests, fresh leaves were cut into pieces, soaked in
methanol in a glass container, kept at room temperature (25 °C) for 72 h, were filtered,
and then the methanol was evaporated [117]. For the fumigant and phytotoxicity bioas-
says of the quassinoids, the extracts are prepared as follows: the roots and leaves are ex-
tracted separately at room temperature—at a dose of 10% w/v—successively with solvents
of increasing polarity [petroleum ether, chloroform, chloroform: methanol (9:1), methanol
and water]. The aqueous leaf extract, more active in bioassays, is fractionated in H2O:
BuOH. The n-butanol extract, which shows activity in the preliminary bioassays, is dis-
solved in methanol and 2 g of this extract is fractionated by gel-permeation chromatog-
raphy on a Sephadex LH-20 column, eluting with MeOH [57].
Figure 1.
The structure of quassinoids isolated from A. altissima. The compound numbers correspond
to the list in Table 1.
Many of the quassinoids could be formed as crystalline matters. Hence, quassinoids
are purifiable phytochemicals [111–113].
For the phytotoxicity and larvicidal tests, fresh leaves were cut into pieces, soaked in
methanol in a glass container, kept at room temperature (25
◦
C) for 72 h, were filtered, and
then the methanol was evaporated [117]. For the fumigant and phytotoxicity bioassays of
the quassinoids, the extracts are prepared as follows: the roots and leaves are extracted
separately at room temperature—at a dose of 10% w/v—successively with solvents of
increasing polarity [petroleum ether, chloroform, chloroform: methanol (9:1), methanol and
water]. The aqueous leaf extract, more active in bioassays, is fractionated in H
2
O:BuOH.
The n-butanol extract, which shows activity in the preliminary bioassays, is dissolved in
methanol and 2 g of this extract is fractionated by gel-permeation chromatography on a
Sephadex LH-20 column, eluting with MeOH [57].
3.5. Biopesticide Potential of Ailanthus altissima and Tests’ Design
3.5.1. Phytotoxicity Assay of Ailanthus altissima
Essential Oil Phytotoxicity
The essential oils of A. altissima negatively affect the seed germination and early-stage
development of the seedlings of the target species. The effect is dose-dependent and is
greater in the light than in the dark. In addition, the phytotoxic effect depends on the
origin of the essential oil, as the oil extracted from flowers is the most phytotoxic [
97
,
98
].
The caryophyllene oxide, b-caryophyllene, germacrene D, and hexahydrofarnesyl acetone
presented in the essential oil may be responsible for such a phytotoxic effect [
98
,
118
,
119
].
Additionally, the complete inhibition of the germination of target plants is achieved after
the application of 400 to 600 µg/mL hydrodistilled leaf residues [97].
Phytotoxicity of Polar Ailanthus altissima Extracts
The juglone index [
120
] of A. altissima has been assessed as very high (0.80–1.40 depending
on the extract concentration [
121
–
123
]. The plant produces allelopathic substances that inhibit

Diversity 2022,14, 680 8 of 16
the seed germination and seedling growth of competing species. They are located mostly in
the bark and the roots, but also occur in the leaves, seeds, and wood. The inhibitor(s) can
readily be extracted from A. altissima with methanol, but not dichloromethane, indicating the
plant’s polar characteristics. The experimental tests show “striking” postemergence effects,
with a nearly complete mortality of all the receiver plant species [124].
The compounds of the methanolic extracts from A. altissima’s fresh leaves and some
sub-fractions have strong inhibitory effects on plant growth. Some fractions show a reg-
ulatory effect on plant by inhibiting the growth of radicles at higher concentrations and
enhancing their growth at lower concentrations [
117
]. The compounds of the aqueous
extracts from A. altissima’s fresh leaves and bark negatively influence the growth of the
treated seedlings of Sinapis alba L. and Brassica napus L. regardless of the dilution [
125
]. The
aqueous extracts of A. altissima leaves have a concentration-dependent herbicidal effect on
Medicago sativa L. seed germination [126].
Ailanthone is highly phytotoxic, with concentrations of 0.7 mL/L causing 50% inhibi-
tion of radicle elongation in a standardized bioassay with garden cress (
Lepidium sativum L.
)
seeds [
127
]. The quassinoids (from the root bark of A. altissima), e.g., ailanthone, ailanthi-
none, and ailanthinol; the alkaloids such as 1-methoxycanthin-6-one; and the phenolic con-
stituents of the leaves are potent phytotoxins [
57
,
97
,
128
–
132
]. A significant pre-emergence
herbicide activity is found for most of the bark dichloromethane extracts, which is di-
rectly correlated with the ailanthone concentration. A remarkable combined pre- and
post-emergence herbicidal activity was found for a specific fraction. These results indicate
that the bark of A. altissima is a potential source for the production of natural herbicides
for use in agriculture [
133
]. Methanol bark extract with the main component ailanthone
was tested for herbicidal effects under field conditions. The results show that it was quite
efficient against the weeds but also caused serious injuries to the crops. Thus, a weak-
ness of ailanthone is its non-selectivity, but a positive feature lies in its ephemeral effects.
Ailanthone is easily degradable by soil microorganisms [
126
,
134
]. It is necessary to note,
however, that ailanthone is an acute toxic triterpene and should be used with caution [
135
].
3.5.2. Antifungal Activity
The antifungal activity test results are contradictory and depend on the extraction
methods and reagents. The methanol and ethanol A. altissima leaves’ extracts have fungici-
dal activity only against Cladosporium cladosporioides of all the tested nine species belonging
to Fusarium,Penicillium,Aspergillus, and Giberella—the toxic microfungi found in cereals
used for livestock and human food. However, this activity is weaker compared to the
Juglans regia leaves’ extracts [
136
]. Ethanol, methanol, and aqueous extracts of A. altissima
were tested against Ceratocystis manginecans (the causal agent of Mango Sudden Death)
using a poisoned food technique and the treatments result in thin, collapsed/damaged
hyphae compared to the control. Phytochemical profiling of the most effective extracts
revealed that 9-octadecanoic acid and I-(+)- ascorbic acid 2, 6-hexadecanoate possibly con-
tribute to the antifungal effect [
137
]. Both acetone and methanol from the leaves’ extracts
have activity against Candida albicans, which is higher than amphotericin B, a gold standard
in antifungal therapy [
87
]. Although C. albicans is not a crop pathogen, the result shows
that further antifungal activity is worth testing. The chloroform extract of Ailanthus excelsa
stem bark shows fungistatic and fungicidal activity against Aspergillus niger,A. fumigatus,
Penicillium frequentence,P. notatum, and Botrytis cinerea [
138
]. It is the quassinoids that have
been found to have inhibitory activities against plant fungal pathogens [139].
3.5.3. Fumigant and Insect Repellent Activity
Essential Oil Fumigant and Insect Repellent Activity
The essential oil of A. altissima bark has a fumigant activity against some pest beetles.
One possible application of A. altissima bark essential oil is for killing insects that damage
stored foods or seeds, as it causes 99.3 and 81.9% mortality to
Oryzaephilus surinamensis
(Linnaeus) (Coleoptera: Silvanidae) and Sitophilus oryzae (Linnaeus) (Coleoptera: Cur-

Diversity 2022,14, 680 9 of 16
culionidae) with within 24 h, respectively [
80
,
140
,
141
]. In addition, Lü and his co-workers
revealed that despite its weak fumigant activity against Tribolium castaneum (Herbst)
(Coleoptera: Tenebrionidae) and Liposcelis paeta Pearman (Psocoptera: Liposcelididae)
adults, it notably repels T. castaneum adults and L. paeta nymphaea [
80
,
140
,
141
]. Addi-
tionally, A. altissima bark oil possesses high fumigant activity against Lasioderma serricorne
(Fabricius 1792) (Coleoptera: Anobiidae) adults with a mortality of 100% at 8
µ
L/L air
within 48 h of exposure; thus, it is obviously a strong repellent of these pests [
142
]. (Z)-
3-hexen-l-ol, which is one of the main components of the essential oil extracted from
A. altissima
stems [
97
], is known as a key herbivore-induced plant volatile. There is no
doubting its role as an indirect defense and this compound is a good candidate for novel
insect pest control strategies [
143
]. Additionally, caryophyllene and caryophyllene oxide,
which are the main constituents of the essential oil of A. altissima leaves and samara [
97
],
are attractive to green lacewings [
144
]. Green lacewing larvae are predators of many soft-
bodied insect pests such as: aphids, thrips, whiteflies, leafhoppers, spider mites (especially
red mites), and mealybugs, and consequently they participate in biological control [
145
].
Caryophyllene and caryophyllene oxide stimulate oviposition in green lacewings, which
leads to increased larval predation against pest insects [
144
]. A. altissima contains com-
pounds with strong acaricidal activity against the parasitic mites that cause skin disease,
namely, Psoroptes cuniculi and Sarcoptes scabiei var. cuniculi [
146
]. It was also found to have
activity towards nematodes of the Meloidogyne genus [147].
Polar Extracts’ Fumigant and Insect-Repellent Activity
The methanol extracts of A. altissima fresh leaves are practically non-toxic to the
mosquito Aedes aegypti larvae [
117
] and the leaves are even used for feeding silkworms [
148
].
However, the methanolic extract of A. altissima leaves causes the malformation and mor-
tality of the larvae of the moth Agrotis ipsilon, (Lepidoptera: Noctuidae), which are
known to cause considerable damage to crops by severing young plants at the ground
level. Aqueus extracts of A. altissima leaves have oviposition-deterrence effects against
Spodoptera frugiperda
(Smith) (Noctuidae), causing delays in the time to pupation and emer-
gence in addition to reduced larval and pupal biomasses [
149
,
150
]. This moth is considered
a noxious pest because the larvae cause massive damage to various crops; consequently,
insecticide sprays are employed against it [
151
]. In addition, 0.5, 1, and 2% ethanol (70%)
extracts of A. altissima bark and leaves have strong antifeeding activity against and signif-
icant insecticidal effects on gypsy moth (Lymantria dispar (L.)) larvae—insects known as
voracious defoliating pests of deciduous trees.
The diethyl ether extract of A. altissima possesses an extremely strong repellent effect
and to a certain extent a contact-killing effect on Oryzaephilus surinamensis (Linnaeus), the
saw-toothed grain beetle [
152
]. The ethanol extract of A. altissima leaves possess strong
acaricidal activity (97.4%) against the spider mite, Tetranychus urticae (Koch), a plant-feeding
mite generally considered to be a pest [
153
]. The extract has no direct toxic effect on the
pest but reduces its fertility about threefold and suppresses the development of larvae from
eggs. The maximum efficiency of the extract was observed after 7–10 days when a filial
generation of the spider mites started developing [154].
Quassinoids extracted both from leaves and roots have insecticidal, antifeedant, and
insect-growth-regulatory activity, and ailanthone, in particular, was found to be efficient
against the aphid Acyrtosiphon pisum [
57
]. There is a high mortality rate of aphids, pests of
peas, when treated with ailanthone [
155
]. Methanol extracts or active substances such as
ailanthone, chaparinone, glaucarubinone, and 13 (18)-dehydroglaucarubinone obtained
from A. altissima leaves can be recommended for the development of new botanical insecti-
cides targeted against the phytophagous larvae of Spodoptera littoralis, a moth referred to
as the African cotton leafworm [
156
]. At the same time, quassinoids seems to be nontoxic
for bees as they are found in propolis [
57
,
134
,
157
–
160
]. In addition, A. altissima bark-based
hexane and methanol extracts do not possess any genotoxic, mutagenic, or carcinogenic

Diversity 2022,14, 680 10 of 16
effects on Saccharomyces cerevisiae, which was used as a test object to evaluate the potential
harm to human health [161].
4. Conclusions
The essential oil and other extracts from A. altissima are quite promising as natural
herbicides. Additionally, the essential oil and other tree-of-heaven compounds have po-
tent fumigant activity. The essential oil and other extracts from A. altissima—as natural
products—are biodegradable and possibly less harmful to human health and to pollinators.
Of course, one should keep in mind that even natural products may have some toxicity; for
instance, carvacrol and thymol aside from their efficacy cannot be considered completely
safe. Even though the hexane and methanol extracts of A. altissima do not possess
in vitro
any genotoxic, mutagenic, or carcinogenic effects, further well-designed tests for both
the pesticidal efficiency and toxicity in humans and pollinators of the essential oils and
quassinoids obtained from this plant are required.
Ideally, effective extraction protocols for industrial yield should be developed so that
both essential oils and quassinoids from A. altissima can be obtained as natural pesticides.
They can help to reduce the use of synthetic pesticides and thereby their negative effects on
wild pollinators and honeybees. Additionally, the intensified harvesting of this aggressive
invasive plant species might contribute to decreasing their populations and reducing their
destructive impact on natural habitats.
Author Contributions:
Conceptualization, E.K. and A.P.; methodology, A.P. and E.K.; validation,
A.P., I.I., Z.N., A.R.A.T. and E.K.; formal analysis, A.P., Z.N. and E.K.; investigation, E.K. and A.P.;
writing—original draft preparation, E.K. and A.P.; writing, review, and editing, E.K., A.P., T.T. and
A.R.A.T.; visualization, A.P. and E.K.; supervision, E.K. and I.I.; project administration, T.T.; funding
acquisition, T.T. All authors have read and agreed to the published version of the manuscript.
Funding:
This work has been carried out in the framework of the National Science Program “Envi-
ronmental Protection and Reduction of Risks of Adverse Events and Natural Disasters”, approved by
the Resolution of the Council of Ministers
№
577/17 August 2018 and supported by the Ministry of
Education and Science (MES) of Bulgaria (Agreement №Д01-279/03 December 2021).
Institutional Review Board Statement: Not applicable.
Informed Consent Statement:
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: The datasets used or analyzed in the current study are available from
the corresponding author on reasonable request. All authors have read and agreed to the published
version of the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Weiss, B.; Amler, S.; Amler, R.W. Pesticides. Pediatrics 2004,113 (Suppl. 4), 1030–1036. [CrossRef] [PubMed]
2.
The Editors of Encyclopaedia Britannica. “Pesticide”. Encyclopedia Britannica, 28 July 2022. Available online: https://www.
britannica.com/technology/pesticide (accessed on 8 August 2022).
3. Alavanja, M.C.; Bonner, M.R. Pesticides and human cancers. Cancer Investig. 2005,23, 700–711. [CrossRef]
4.
Costa, L.G.; Giordano, G.; Guizzetti, M.; Vitalone, A. Neurotoxicity of pesticides: A brief review. Front. Biosci.
2008
,13, 1240–1249.
[CrossRef]
5.
Damalas, C.A.; Eleftherohorinos, I.G. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Public
Health 2011,8, 1402–1419. [CrossRef] [PubMed]
6.
Suratman, S.; Edwards, J.W.; Babina, K. Organophosphate pesticides exposure among farmworkers: Pathways and risk of adverse
health effects. Rev. Environ. Health 2015,30, 65–79. [CrossRef]
7.
Li, Z.; Jennings, A. Worldwide regulations of standard values of pesticides for human health risk control: A Review. Int. J. Environ.
Res. Public Health 2017,14, 826. [CrossRef]
8.
Kim, K.H.; Kabir, E.; Jahan, S.A. Exposure to pesticides and the associated human health effects. Sci. Total Environ.
2017
,1,
525–535. [CrossRef]
9. Landrigan, P.J. Pesticides and Human Reproduction. JAMA Intern. Med. 2018,178, 26–27. [CrossRef]

Diversity 2022,14, 680 11 of 16
10.
Adeyemi, J.A.; Ukwenya, V.O.; Arowolo, O.K.; Olise, C.C. Pesticides-induced Cardiovascular Dysfunctions: Prevalence and
Associated Mechanisms. Curr. Hypertens. Rev. 2021,17, 27–34. [CrossRef]
11.
Needleman, H.L.; Gunnoe, C.; Leviton, A.; Reed, R.; Peresie, H.; Maher, C.; Barrett, P. Deficits in psychologic and classroom
performance of children with elevated dentine lead levels. N. Engl. J. Med. 1979,300, 689–695. [CrossRef]
12.
FAO. Pollinators Vital to Our Food Supply under Threat. 2021. Available online: http://www.fao.org/news/story/en/item/38
4726/icode/ (accessed on 25 July 2021).
13.
Biesmeijer, J.C.; Roberts, S.P.M.; Reemer, M.; Ohlemüller, R.; Edwards, M.; Peeters, T.; Schaffers, A.P.; Potts, S.G.; Kleukers, R.;
Thomas, C.D.; et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science
2006
,313,
351–354. [CrossRef]
14. Brown, M.J.; Paxton, R.J. The conservation of bees: A global perspective. Apidologie 2009,40, 410–416. [CrossRef]
15.
Potts, S.; Biesmeijer, K.; Bommarco, R.; Breeze, T.; Carvalheiro, L.; Franzén, M.; González-Varo, J.P.; Holzschuh, A.; Kleijn, D.;
Klein, A.-M.; et al. Status and Trends of European Pollinators. Key Findings of the STEP Project; Pensoft Publishers: Sofia, Bulgaria,
2015; p. 72.
16.
Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W.E. Global pollinator declines: Trends, impacts and
drivers. Trends Ecol. Evol. 2010,25, 345–353. [CrossRef]
17.
Carvalheiro, L.G.; Kunin, W.E.; Keil, P.; Aguirre-Gutiérrez, J.; Ellis, W.N.; Fox, R.; Biesmeijer, J.C. Species richness declines and
biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 2013,16, 870–878. [CrossRef]
18.
Ollerton, J.; Erenler, H.; Edwards, M.; Crockett, R. Extinctions of aculeate pollinators in Britain and the role of large-scale
agricultural changes. Science 2014,346, 1360–1362. [CrossRef]
19.
Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee declines driven by combined stress from parasites, pesticides, and lack of
flowers. Science 2015,347, 1255957. [CrossRef]
20. Goulson, D.; Frey, H.; Tzinieris, S.; Callaghan, C.; Kerr, J. Call to restrict neonicotinoids. Science 2018,360, 973. [CrossRef]
21.
Wright, G.A.; Softley, S.; Earnshaw, H. Low doses of neonicotinoid pesticides in food rewards impair short-term olfactory memory
in foraging-age honeybees. Sci. Rep. 2015,5, 15322. [CrossRef]
22.
Stanley, D.A.; Smith, K.E.; Raine, N.E. Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid
pesticide. Sci. Rep. 2015,5, 16508. [CrossRef]
23.
Stanley, D.A.; Garratt, M.P.; Wickens, J.B.; Wickens, V.J.; Potts, S.G.; Raine, N.E. Neonicotinoid pesticide exposure impairs crop
pollination services provided by bumblebees. Nature 2015,528, 548–550. [CrossRef]
24.
Woodcock, B.A.; Isaac, N.J.; Bullock, J.M.; Roy, D.B.; Garthwaite, D.G.; Crowe, A.; Pywell, R.F. Impacts of neonicotinoid use on
long-term population changes in wild bees in England. Nat. Commun. 2016,7, 12459. [CrossRef] [PubMed]
25.
Sánchez-Bayo, F.; Goulson, D.; Pennacchio, F.; Nazzi, F.; Goka, K.; Desneux, N. Are bee diseases linked to pesticides?—A brief
review. Environ. Int. 2016,89, 7–11. [CrossRef] [PubMed]
26.
Ramos-Jiliberto, R.; de Espanés, P.M.; Vázquez, D.P. Pollinator declines and the stability of plant–pollinator networks. Ecosphere
2020,11, e03069. [CrossRef]
27.
Althaus, S.L.; Berenbaum, M.R.; Jordan, J.; Shalmon, D.A. No buzz for bees: Media coverage of pollinator decline. Proc. Natl.
Acad. Sci. USA 2021,118, e2002552117. [CrossRef]
28.
Whitehorn, P.R.; O’connor, S.; Wackers, F.L.; Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen
production. Science 2012,336, 351–352. [CrossRef]
29.
Boily, M.; Sarrasin, B.; DeBlois, C.; Aras, P.; Chagnon, M. Acetylcholinesterase in honey bees (Apis mellifera) exposed to
neonicotinoids, atrazine and glyphosate: Laboratory and field experiments. Environ. Sci. Pollut. Res.
2013
,20, 5603–5614.
[CrossRef]
30.
Goulson, D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol.
2013
,50, 977–987.
[CrossRef]
31.
Botías, C.; David, A.; Horwood, J.; Abdul-Sada, A.; Nicholls, E.; Hill, E.; Goulson, D. Neonicotinoid residues in wildflowers, a
potential route of chronic exposure for bees. Environ. Sci. Technol. 2015,49, 12731–12740. [CrossRef]
32.
Main, A.R.; Hladik, M.L.; Webb, E.B.; Goyne, K.W.; Mengel, D. Beyond neonicotinoids–Wild pollinators are exposed to a range of
pesticides while foraging in agroecosystems. Sci. Total Environ. 2020,742, 140436. [CrossRef]
33.
English, S.G.; Sandoval-Herrera, N.I.; Bishop, C.A.; Cartwright, M.; Maisonneuve, F.; Elliott, J.E.; Welch, K.C. Neonicotinoid
pesticides exert metabolic effects on avian pollinators. Sci. Rep. 2021,11, 2914. [CrossRef]
34.
Chan, D.S.W.; Raine, N.E. Population decline in a ground-nesting solitary squash bee (Eucera pruinosa) following exposure to a
neonicotinoid insecticide treated crop (Cucurbita pepo). Sci. Rep. 2021,11, 4241. [CrossRef] [PubMed]
35.
Bloom, E.H.; Wood, T.J.; Hung, K.L.J.; Ternest, J.J.; Ingwell, L.L.; Goodell, K.; Szendrei, Z. Synergism between local- and
landscape-level pesticides reduces wild bee floral visitation in pollinator-dependent crops. J. Appl. Ecol.
2021
,58, 1187–1198.
[CrossRef]
36.
Aktar, M.W.; Sengupta, D.; Chowdhury, A. Impact of pesticides use in agriculture: Their benefits and hazards. Interdiscip. Toxicol.
2009,2, 1–12. [CrossRef]
37.
Abraham, J.; Benhotons, G.S.; Krampah, I.; Tagba, J.; Amissah, C.; Abraham, J.D. Commercially formulated glyphosate can kill
non-target pollinator bees under laboratory conditions. Entomol. Exp. Appl. 2018,166, 695–702. [CrossRef]

Diversity 2022,14, 680 12 of 16
38.
Vázquez, D.E.; Balbuena, M.S.; Chaves, F.; Gora, J.; Menzel, R.; Farina, W.M. Sleep in honey bees is affected by the herbicide
glyphosate. Sci. Rep. 2020,10, 10516. [CrossRef]
39.
Vázquez, D.E.; Ilina, N.; Pagano, E.A.; Zavala, J.A.; Farina, W.M. Glyphosate affects the larval development of honey bees
depending on the susceptibility of colonies. PLoS ONE 2018,13, e0205074. [CrossRef]
40.
Haas, J.; Nauen, R. Pesticide risk assessment at the molecular level using honey bee cytochrome P450 enzymes: A complementary
approach. Environ. Int. 2021,147, 106372. [CrossRef]
41.
Battisti, L.; Potrich, M.; Sampaio, A.R.; de Castilhos Ghisi, N.; Costa-Maia, F.M.; Abati, R.; Sofia, S.H. Is glyphosate toxic to bees?
A meta-analytical review. Sci. Total Environ. 2021,767, 145397. [CrossRef]
42.
Hipólito, J.; Coutinho, J.; Mahlmann, T.; Santana, T.B.R.; Magnusson, W.E. Legislation and pollination: Recommendations for
policymakers and scientists. Perspect. Ecol. Conserv. 2021,19, 1–9. [CrossRef]
43.
Gemmill-Herren, B.; Garibaldi, L.A.; Kremen, C.; Ngo, H.T. Building effective policies to conserve pollinators: Translating
knowledge into policy. Curr. Opin. Insect. Sci. 2021,46, 64–71. [CrossRef]
44.
Shaaya, E.; Ravid, U.; Paster, N.; Juven, B.; Zisman, U.; Pissarev, V. Fumigant toxicity of essential oils against four major
stored-product insects. J. Chem. Ecol. 1991,17, 499–504. [CrossRef]
45. Isman, M.B. Plant essential oils for pest and disease management. J. Crop Prot. 2000,19, 603–608. [CrossRef]
46.
Suthisut, D.; Fields, P.G.; Chandrapatya, A. Fumigant toxicity of essential oils from three Thai plants (Zingiberaceae) and their
major compounds against Sitophilus zeamais,Tribolium castaneum and two parasitoids. J. Stored Prod. Res.
2011
,47, 222–230.
[CrossRef]
47.
Polato˘glu, K.; Karakoç, Ö.C.; Gören, N. Phytotoxic, DPPH scavenging, insecticidal activities and essential oil composition of
Achillea vermicularis,A. teretifolia and proposed chemotypes of A. biebersteinii (Asteraceae). Ind. Crops Prod.
2013
,51, 35–45.
[CrossRef]
48.
de Elguea-Culebras, G.O.; Sánchez-Vioque, R.; Berruga, M.I.; Herraiz-Peñalver, D.; Santana-Méridas, O. Antifeedant effects
of common terpenes from Mediterranean aromatic plants on Leptinotarsa decemlineata.J. Plant Nutr. Soil Sci.
2017
,17, 475–485.
[CrossRef]
49.
Dudai, N.; Poljakoff-Mayber, A.; Mayer, A.M.; Putievsky, E.; Lerner, H.R. Essential oils as allelochemicals and their potential use
as bioherbicides. J. Chem. Ecol. 1999,25, 1079–1089. [CrossRef]
50. Tworkoski, T. Herbicide effects of essential oils. Weed Sci. 2002,50, 425–431. [CrossRef]
51.
Angelini, L.G.; Carpanese, G.; Cioni, P.L.; Morelli, I.; Macchia, M.; Flamini, G. Essential oils from Mediterranean Lamiaceae as
weed germination inhibitors. J. Agric. Food Chem. 2003,51, 6158–6164. [CrossRef]
52.
Kordali, S.; Cakir, A.; Ozer, H.; Cakmakci, R.; Kesdek, M.; Mete, E. Antifungal, phytotoxic and insecticidal properties of essential
oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene. Bioresour. Technol.
2008
,
99, 8788–8795. [CrossRef]
53.
Haig, T.J.; Haig, T.J.; Seal, A.N.; Pratley, J.E.; An, M.; Wu, H. Lavender as a source of novel plant compounds for the development
of a natural herbicide. J. Chem. Ecol. 2009,35, 1129–1136. [CrossRef]
54.
Verdeguer, M.; Blázquez, M.A.; Boira, H. Phytotoxic effects of Lantana camara,Eucalyptus camaldulensis and Eriocephalus africanus
essential oils in weeds of Mediterranean summer crops. Biochem. Syst. Ecol. 2009,37, 362–369. [CrossRef]
55.
De Almeida, L.F.R.; Frei, F.; Mancini, E.; De Martino, L.; De Feo, V. Phytotoxic activities of Mediterranean essential oils. Molecules
2010,15, 4309–4323. [CrossRef]
56. Wright, C.; Chhetri, B.K.; Setzer, W.N. Chemical composition and phytotoxicity of the essential oil of Encelia farinosa growing in
the Sonoran Desert. Am. J. Essent. Oil. Nat. Prod. 2013,1, 18–22.
57.
De Feo, V.; Mancini, E.; Voto, E.; Curini, M.; Digilio, M.C. Bioassay-oriented isolation of an insecticide from Ailanthus altissima.
J. Plant Interact. 2009,4, 119–123. [CrossRef]
58.
He, C.; Wang, Y.; Yang, T.; Wang, H.; Liao, H.; Liang, D. Quassinoids with insecticidal activity against diaphorina citri kuwayama
and neuroprotective activities from Picrasma quassioides.J. Agric. Food Chem. 2019,68, 117–127. [CrossRef]
59.
Fang, X.; Di, Y.T.; Zhang, Y.; Xu, Z.P.; Lu, Y.; Chen, Q.Q.; Zheng, Q.T.; Hao, X.J. Unprecedented quassinoids with promising
biological activity from Harrisonia perforata.Angew. Chem. Int. Ed. 2015,54, 5592–5595. [CrossRef]
60.
Kowarik, I.; Säumel, I. Biological flora of central Europe: Ailanthus altissima (Mill.) swingle. Perspect. Plant Ecol. Evol. Syst.
2007
,8,
207–237. [CrossRef]
61. DAISIE. Handbook of Alien Species in Europe; Springer: Dordrecht, The Netherlands, 2009. [CrossRef]
62.
Petrova, A.; Vladimirov, V.; Georgiev, V. Invasive Alien Plant Species in Bulgaria; Institute of Biodiversity and Ecosystem Research,
Bulgarian Academy of Sciences: Sofia, Bulgaria, 2012. (In Bulgarian)
63.
Zahariev, D. Invasive plant species along the major rivers in Strandzha Natural Park. In Proceedings of the Seminar of Ecology—2014,
Sofia, Bulgaria, 24–25 April 2014; pp. 148–158.
64. Monaco, A. European Guidelines on Protected Areas and Invasive Alien Species; Council of Europe: Rome, Italy, 2014.
65.
Sladonja, B.; Sušek, M.; Guillermic, J. Review on invasive tree of heaven (Ailanthus altissima (Mill.) Swingle) conflicting values:
Assessment of its ecosystem services and potential biological threat. Environ. Manag. 2015,56, 1009–1034. [CrossRef]
66.
Global Invasive Species Database. Species Profile: Ailanthus altissima. 2019. Available online: http://www.iucngisd.org/gisd/
species.php?sc=319 (accessed on 25 July 2022).

Diversity 2022,14, 680 13 of 16
67.
Domina, G. Invasive Aliens in Italy: Enumeration, History, Biology and Their Impact. In Invasive Alien Species: Observations
and Issues from Around the World; Pullaiah, T., Ielmini, M.R., Eds.; John Wiley & Sons Ltd.: Hoboken, NJ, USA, 2021; Volume 3,
pp. 190–214. [CrossRef]
68.
Demeter, A.; Saláta, D.; TormánéKovács, E.; Szirmai, O.; Trenyik, P.; Meinhardt, S.; Czóbel, S. Effects of the Invasive Tree Species
Ailanthus altissima on the Floral Diversity and Soil Properties in the Pannonian Region. Land 2021,10, 1155. [CrossRef]
69.
Motti, R.; Zotti, M.; Bonanomi, G.; Cozzolino, A.; Stinca, A.; Migliozzi, A. Climatic and anthropogenic factors affect
Ailanthus altissima invasion in a Mediterranean region. Plant Ecol. 2021,222, 1347–1359. [CrossRef]
70.
Terzi, M.; Fontaneto, D.; Casella, F. Effects of Ailanthus altissima Invasion and Removal on High-Biodiversity Mediterranean
Grasslands. Environ. Manag. 2021,68, 914–927. [CrossRef]
71.
Pedersini, C.; Bergamin, M.; Aroulmoji, V.; Baldini, S.; Picchio, R.; Pesce, P.G.; Ballarin, L.; Murano, E. Herbicide Activity of
Extracts from Ailanthus altissima (Simaroubaceae). Nat. Prod. Commun. 2011,6, 593–596. [CrossRef]
72.
Kubota, K.; Fukamiya, N.; Hamada, T.; Okano, M.; Tagahara, K.; Lee, K.H. Two new quassinoids, ailantinols A and B, and related
compounds from Ailanthus altissima.J. Nat. Prod. 1996,59, 683–686. [CrossRef]
73.
Kubota, K.; Fukamiya, N.; Okano, M.; Tagahara, K.; Lee, K.H. Two new quassinoids, ailantinols C and D, from Ailanthus altissima.
Bull. Chem. Soc. Jpn. 1996,69, 3613–3617. [CrossRef]
74.
Tamura, S.; Fukamiya, N.; Okano, M.; Koyama, J.; Koike, K.; Tokuda, H.; Nishino, H. Three new quassinoids, ailantinol E, F, and
G, from Ailanthus altissima.Chem. Pharm. Bull. 2003,51, 385–389. [CrossRef]
75.
Takeya, K.; Kobata, H.; Ozeki, A.; Morita, H.; Itokawa, H. A new quassinoid from Ailanthus vilmoriniana.J. Nat. Prod.
1997
,60,
642–644. [CrossRef]
76. Joshi, B.C.; Pandey, A.; Sharma, R.P.; Khare, A. Quassinoids from Ailanthus excelsa.Phytochemistry 2003,62, 579–584. [CrossRef]
77.
Manimaran, V.; Suganthy, M.; Balasubramanian, A.; Kumar, P.P. Management of tea mosquito bug, Helopeltis antonii Signoret
infesting Ailanthus excelsa Roxb. J. Entomol. Zool. Stud. 2019,7, 620–623.
78.
Karalija, E.; Dahija, S.; Pari´c, A.; Zeljkovi´c, S. ´
C. Phytotoxic potential of selected essential oils against Ailanthus altissima (Mill.)
Swingle, an invasive tree. Sust. Chem. Pharm. 2020,15, 100219. [CrossRef]
79.
Li, X.; Li, Y.; Ma, S.; Zhao, Q.; Wu, J.; Duan, L.; Wang, S. Traditional uses, phytochemistry, and pharmacology of Ailanthus altissima
(Mill.) Swingle bark: A comprehensive review. J. Ethnopharmacol. 2021,275, 114121. [CrossRef]
80.
Lü, J.H.; He, Y.Q. Fumigant toxicity of Ailanthus altissima Swingle, Atractylodes lancea (Thunb.) DC. and Elsholtzia stauntonii Benth
extracts on three major stored-grain insects. Ind. Crops Prod. 2010,32, 681–683. [CrossRef]
81.
Ohmoto, T.; Koike, K.; Sakamoto, Y. Studies on the constituents of A. altissima Swingle II. The alkaloid constituent. Chem. Pharm.
Bull. 1981,29, 390–395. [CrossRef]
82.
Ohmoto, T.; Koike, K. Studies on the constituents of A. altissima Swingle III. The alkaloid constituents. Chem. Pharm. Bull.
1984
,
32, 170–173. [CrossRef]
83.
Masteli´c, J.; Jerkovi´c, I. Volatile Constituents from the Leaves of Young and Old Ailanthus altissima (Mili.) Swingle Tree. Croat.
Chem. Acta 2002,75, 189–197.
84.
Kozuharova, E.; Lebanova, H.; Getov, I.; Benbassat, N.; Kochmarov, V. Ailanthus altissima (Mill.) Swingle—A terrible invasive pest
in Bulgaria or potential useful medicinal plant? Bothalia 2014,44, 213–230.
85.
Zhelev, I.; Georgiev, K.; Dimitrova-Dyulgerova, I. Carotenoid profile of Ailanthus altissima stem bark, in-vitro antioxidant and
antineoplastic activities. World J. Pharm. Res. 2016,5, 1816.
86.
Cho, S.K.; Jeong, M.; Jang, D.S.; Choi, J.H. Anti-inflammatory Effects of Canthin-6-one Alkaloids from Ailanthus altissima.Planta
Med. 2018,50, 527–535. [CrossRef]
87.
Poljuha, D.; Sladonja, B.; Šola, I.; Dudaš, S.; Bili´c, J.; Rusak, G.; Eloff, J.N. Phenolic composition of leaf extracts of
Ailanthus altissima
(Simaroubaceae) with antibacterial and antifungal activity equivalent to standard antibiotics. Nat. Prod. Commun.
2017
,12,
1934578X1701201021. [CrossRef]
88.
Du, Y.Q.; Yan, Z.Y.; Shi, S.C.; Hou, Z.L.; Huang, X.X.; Song, S.J. Benzoic acid derivatives from the root barks of Ailanthus altissima.
J. Asian Nat. Prod. Res. 2021,23, 103–109. [CrossRef]
89.
Du, Y.Q.; Yan, Z.Y.; Chen, J.J.; Wang, X.B.; Huang, X.X.; Song, S.J. The identification of phenylpropanoids isolated from the root
bark of Ailanthus altissima (Mill.) Swingle. Nat. Prod. Res. 2021,35, 1139–1146. [CrossRef]
90.
Du, Y.Q.; Bai, M.; Yu, X.Q.; Lv, T.M.; Lin, B.; Huang, X.X.; Song, S.J. Quassinoids from the Root Barks of Ailanthus altissima:
Isolation, Configurational Assignment, and Cytotoxic Activities. Chin. J. Chem. 2021,39, 879–886. [CrossRef]
91.
Wang, C.M.; Li, H.F.; Wang, X.K.; Li, W.G.; Su, Q.; Xiao, X.; Zhang, C.H. Ailanthus altissima-derived ailanthone enhances gastric
cancer cell apoptosis by inducing the repression of base excision repair by downregulating p23 Expression. Int. J. Biol. Sci.
2021
,
17, 2811. [CrossRef] [PubMed]
92.
Duan, Z.K.; Lin, B.; Du, Y.Q.; Li, C.; Yu, X.Q.; Xue, X.B.; Huang, X.X. Monoterpenoid coumarins and monoterpenoid phenyl-
propanoids from the root bark of Ailanthus altissima.New J. Chem. 2021,45, 1100–1108. [CrossRef]
93.
Caramelo, D.; Pedro, S.I.; Marques, H.; Simão, A.Y.; Rosado, T.; Barroca, C.; Gallardo, E. Insights into the Bioactivities and
Chemical Analysis of Ailanthus altissima (Mill.) Swingle. Appl. Sci. 2021,11, 11331. [CrossRef]
94.
Bray, D.H.; Boardman, P.; ONeill, M.J.; Chan, K.L.; Phillipson, J.D.; Warhurst, D.C.; Suffness, M. Plants as a source of antimalarial
drugs 5. Activities of Ailanthus altissima stem constituents and of some related quassinoids. Phytother. Res.
1987
,1, 22–24.
[CrossRef]

Diversity 2022,14, 680 14 of 16
95.
Okunade, A.L.; Bikoff, R.E.; Casper, S.J.; Oksman, A.; Goldberg, D.E.; Lewis, W.H. Antiplasmodial activity of extracts and
quassinoids isolated from seedlings of Ailanthus altissima (Simaroubaceae). Phytother. Res. 2003,17, 675–677. [CrossRef]
96.
Li, Y.; Zhao, M.; Zhang, Z. Quantitative proteomics reveals the antifungal effect of canthin-6-one isolated from Ailanthus altissima
against Fusarium oxysporum f. sp. cucumerinum in vitro. PLoS ONE 2021,16, e0250712. [CrossRef]
97.
Albouchi, F.; Hassen, I.; Casabianca, H.; Hosni, K. Phytochemicals, antioxidant, antimicrobial and phytotoxic activities of
Ailanthus altissima (Mill.) Swingle leaves. S. Afr. J. Bot. 2013,87, 164–174. [CrossRef]
98.
El Ayeb-Zakhama, A.; Ben Salem, S.; Sakka-Rouis, L.; Flamini, G.; Ben Jannet, H.; Harzallah-Skhiri, F. Chemical Composition and
phytotoxic effects of essential oils obtained from Ailanthus altissima (Mill.) Swingle cultivated in Tunisia. Chem. Biodivers.
2014
,11,
1216–1227. [CrossRef]
99.
Kozuharova, E.; Benbassat, N.; Berkov, S.; Ionkova, I. Ailanthus altissima and Amorpha fruticosa—Invasive arboreal alien plants as
cheap sources of valuable essential oils. Pharmacia 2020,67, 71. [CrossRef]
100.
Lü, J.; Wu, S. Bioactivity of essential oil from Ailanthus altissima bark against 4 major stored-grain insects. Afr. J. Microbiol. Res.
2010,4, 154–157. [CrossRef]
101.
Zhou, L.; Wang, J.; Wang, K.; Xu, J.; Zhao, J.; Shan, T.; Luo, C. Secondary metabolites with antinematodal activity from higher
plants. In Studies in Natural Products Chemistry; Elsevier: Amsterdam, The Netherlands, 2012; Volume 37, pp. 67–114. [CrossRef]
102.
He, Q.; Xiao, H.; Li, J.; Liu, Y.; Jia, M.; Wang, F.; Zhang, Y.; Wang, W.; Wang, S. Fingerprint analysis and pharmacological
evaluation of Ailanthus altissima.Int. J. Mol. Med. 2018,41, 3024–3032. [CrossRef] [PubMed]
103.
Wang, R.X.; Mao, X.X.; Zhou, J.; Zhang, M.L.; Wu, Y.B.; Huo, C.H.; Gu, Y.C. Antitumor activities of six quassinoids from
Ailanthus altissima.Chem. Nat. Compd. 2017,53, 28–32. [CrossRef]
104.
Wang, Y.; Wang, W.J.; Su, C.; Zhang, D.M.; Xu, L.P.; He, R.R.; Ye, W.C. Cytotoxic quassinoids from Ailanthus altissima.Bioorg. Med.
Chem. Lett. 2013,23, 654–657. [CrossRef]
105.
Naora, H.; Ishibashi, M.; Furuno, T.; Tsuyuki, T.; Murae, T.; Hirota, H.; Takahashi, T.; Itai, A.; Iitaka, Y. Structure determination of
bitter principles in Ailanthus altissima. Structure of shinjulactone A and revised structure of ailanthone. Bull. Chem. Soc. Jpn.
1983
,
56, 3694–3698. [CrossRef]
106.
Tamura, S.; Fukamiya, N.; Okano, M.; Koike, K. A new quassinoid, ailantinol H from Ailanthus altissima.Nat. Prod. Res.
2006
,20,
1105–1109. [CrossRef]
107.
Ishibashi, M.; Tsuyuki, T.; Murae, T.; Hirota, H.; Takahashi, T.; Itai, A.; Iitaka, Y. Constituents of the Root Bark of Ailanthus altissima
S WINGLE. Isolation and X-Ray Crystal Structures of Shinjudilactone and Shinjulactone C and Conversion of Ailanthone into
Shinjudilactone. Bull. Chem. Soc. Jpn. 1983,56, 3683–3693. [CrossRef]
108.
Yoshimura, S.; Ishibashi, M.; Tsuyuki, T.; Takahashi, T.; Matsushita, K. Constituents of seeds of Ailanthus altissima Swingle.
Isolation and structures of shinjuglycosides A, B, C, and D. Bull. Chem. Soc. Jpn. 1984,57, 2496–2501. [CrossRef]
109.
Niimi, Y.; Tsuyuki, T.; Takahashi, T.; Matsushita, K. Bitter principles of Ailanthus altissima Swingle. Structure determination of
shinjuglycosides E and F. Chem. Pharm. Bull. 1987,35, 4302–4306. [CrossRef]
110.
Furuno, T.; Ishibashi, M.; Naora, H.; Murae, T.; Hirota, H.; Tsuyuki, T.; Iitaka, Y. Structure determination of bitter principles of
Ailanthus altissima. Structures of shinjulactones B, D, and E. Bull. Chem. Soc. Jpn. 1984,57, 2484–2489. [CrossRef]
111.
Ishibashi, M.; Yoshimura, S.; Tsuyuki, T.; Takahashi, T.; Itai, A.; Iitaka, Y. Structure determination of bitter principles of
Ailanthus altissima. Structures of shinjulactones F, I, J, and K. Bull. Chem. Soc. Jpn. 1984,57, 2885–2892. [CrossRef]
112.
Ishibashi, M.; Yoshimura, S.; Tsuyuki, T.; Takahashi, T.; Matsushita, K. Shinjulactones G and H, new bitter principles of
Ailanthus altissima Swingle. Bull. Chem. Soc. Jpn. 1984,57, 2013–2014. [CrossRef]
113.
Ishibashi, M.; Tsuyuki, T.; Takahashi, T. Structure determination of a new bitter principle, shinjulactone L, from Ailanthus altissima.
Bull. Chem. Soc. Jpn. 1985,58, 2723–2724. [CrossRef]
114.
Niimi, Y.; Tsuyuki, T.; Takahashi, T.; Matsushita, K. Structure determination of shinjulactones M and N, new bitter principles from
Ailanthus altissima Swingle. Bull. Chem. Soc. Jpn. 1986,59, 1638–1640. [CrossRef]
115.
Yang, X.L.; Yuan, Y.L.; Zhang, D.M.; Li, F.; Ye, W.C. Shinjulactone O, a new quassinoid from the root bark of Ailanthus altissima.
Nat. Prod. Res. 2014,28, 1432–1437. [CrossRef]
116.
Tan, Q.W.; Ni, J.C.; Zheng, L.P.; Fang, P.H.; Shi, J.T.; Chen, Q.J. Anti-Tobacco mosaic virus quassinoids from Ailanthus altissima
(Mill.) Swingle. J. Agric. Food Chem. 2018,66, 7347–7357. [CrossRef]
117.
Tsao, R.; Romanchuk, F.E.; Peterson, C.J.; Coats, J.R. Plant growth regulatory effect and insecticidal activity of extracts of tree of
Heaven (Ailanthus altissima L.). BMC Ecol.
2002
,2, 1. Available online: https://bmcecol.biomedcentral.com/articles/10.1186/14
72-6785-2-1 (accessed on 25 July 2022).
118.
Quintana, N.; El Kassis, E.G.; Stermitz, F.R.; Vivanco, J.M. Phytotoxic compounds from roots of Centaurea diffusa Lam. Plant Signal.
Behav. 2009,4, 9–14. [CrossRef]
119.
De Martino, L.; Formisano, C.; Mancini, E.; Feo, V.D.; Piozzi, F.; Rigano, D.; Senatore, F. Chemical composition and phytotoxic
effects of essential oils from four Teucrium species. Nat. Prod. Commun. 2010,5, 1969–1976. [CrossRef]
120.
Szabó, L. Juglone index—A possibility for expressing allelopathic potential of plant taxa with various life strategies. Acta Bot.
Hung. 1999,42, 295–305.
121.
Csiszár, Á. Allelopathic effects of invasive woody plant species in Hungary. Acta Silv. Lignaria Hung.
2009
,5, 9–17. Available
online: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.1066.4899&rep=rep1&type=pdf (accessed on 25 July 2022).

Diversity 2022,14, 680 15 of 16
122.
Csiszár, Á.; Korda, M.; Schmidt, D.; Šporˇci´c, D.; Süle, P.; Teleki, B.; Tiborcz, V.; Zagyvai, G.; Bartha, D. Allelopathic potential of
some invasive plant species occurring in Hungary. Allelopath. J. 2013,31, 309–318.
123.
Novak, N.; Novak, M.; Bari´c, K.; Š´cepanovi´c, M.; Ivi´c, D. Allelopathic potential of segetal and ruderal invasive alien plants.
J. Cent. Eur. Agric. 2018,19, 408–422. [CrossRef]
124.
Heisy, R. Allelopathic and herbicidal effects of extracts from tree of heaven (Ailanthus altissima). Am. J. Bot.
1990
,77, 662–670.
[CrossRef]
125.
Bostan, C.; Borlea, F.; Mihoc, C.; Selesan, M. Ailanthus altissima species invasion on biodiversity caused by potential allelopathy.
J. Agric. Sci.
2014
,46, 95–103. Available online: http://cormoran.portiledefier.ro/wp-content/uploads/2013/02/bostan_cristian_
1.pdf (accessed on 25 July 2022).
126.
Sladonja, B.; Pohulja, D.; Sušek, M.; Dudaš, S. Herbicidal effect of Ailanthus altissima leaves water extracts on Medicago sativa seeds
germination. In Book of Abstracts of the 3rd Conference with International Participation Conference VIVUS; Biotechnical Centre Naklo:
Naklo, Slovenia, 2014; pp. 476–481. Available online: http://civ.iptpo.hr/wp-content/uploads/publikacije/Znanstveni%20rad%
20u%20zborniku%20skupa_VIVUS_2014.pdf (accessed on 25 July 2022).
127.
Heisey, R.M. Identification of an allelopathic compound from Ailanthus altissima (Simaroubaceae) and characterization of its
herbicidal activity. Am. J. Bot. 1996,83, 192–200. [CrossRef]
128.
Casinovi, C.G.; Ceccherelli, P.; Fardella, G.; Grandolini, G. Isolation and structure of a quassinoid from Ailanthus glandulosa.
Phytochemistry 1983,22, 2871–2873. [CrossRef]
129.
Lin, L.-J.; Peiser, G.; Ying, B.-P.; Mathias, K.; Karasina, F.; Wang, Z.; Itatani, J.; Green, L.; Hwang, Y.-S. Identification of plant
growth inhibitory principles in Ailanthus altissima and Castela tortuosa.J. Agric. Food Chem. 1995,43, 1706–1711. [CrossRef]
130.
De Feo, V.; De Martino, L.; Quaranta, E.; Pizza, C. Isolation of phytotoxic compounds from tree-of-heaven (Ailanthus altissima
Swingle). J. Agric. Food Chem. 2003,51, 1177–1180. [CrossRef]
131.
De Feo, V.; Martino, L.D.; Santoro, A.; Leone, A.; Pizza, C.; Franceschelli, S.; Pascale, M. Antiproliferative effects of tree-of-heaven
(Ailanthus altissima Swingle). Phytother. Res. 2005,19, 226–230. [CrossRef]
132.
Lebedev, V.G.; Krutovsky, K.V.; Shestibratov, K.A. Fell Upas Sits, the Hydra-Tree of Death
†
, or the Phytotoxicity of Trees. Molecules
2019,24, 1636. [CrossRef] [PubMed]
133.
Borchardt, J.R.; Wyse, D.L.; Sheaffer, C.C.; Kauppi, K.L.; Fulcher, R.G.; Ehlke, N.J.; Biesboer, D.D.; Bey, R.F. Antimicrobial activity
of native and naturalized plants of Minnesota and Wisconsin. J. Med. Plant Res. 2008,2, 98–110. [CrossRef]
134.
Heisey, R.M.; Heisey, T.K. Herbicidal effects under field conditions of Ailanthus altissima bark extract, which contains ailanthone.
Plant Soil 2003,256, 85–99. [CrossRef]
135.
Anonymous. National Center for Biotechnology Information. PubChem Database. Ailanthone, CID=72965; 2019. Available
online: https://pubchem.ncbi.nlm.nih.gov/compound/Ailanthone (accessed on 1 January 2022).
136.
Balkan, B.; Balkan, S.; Aydo˘gdu, H.; Özcan, Ö. Antifungal activities of Ailanthus altissima Swingle and
Juglans regia
L. leaves
against some cereal fungi. J. Appl. Environ. Biol. Sci. 2014,8, 76–79.
137.
Jabeen, K.; Asad, S.; Zakria, M. Antifungal Evaluation and Phytochemical Identification of Selected Botanicals against
Ceratocystis manginecans Causing Mango Sudden Death. J. Plant Pathol. Microbiol. 2018,9, 465. [CrossRef]
138.
Joshi, B.C.; Pandey, A.; Chaurasia, L.; Pal, M.; Sharma, R.P.; Khare, A. Antifungal activity of the stem bark of Ailanthus excelsa.
Fitoterapia 2003,74, 689–691. [CrossRef]
139.
Chen, J.J.; Bai, W.; Lu, Y.B.; Feng, Z.Y.; Gao, K.; Yue, J.M. Quassinoids with Inhibitory Activities against Plant Fungal Pathogens
from Picrasma javanica.J. Nat. Prod. 2021,84, 2111–2120. [CrossRef]
140.
Lü, J. The insecticidal activities of Ailanthus altissima extracts on several kinds of important stored-grain insects. Grain Storage
2007,36, 17–20.
141. Lü, J.H.; Lu, Y.J.; Hu, Y.Y. Controlling effects of three plant essential oils on Liposcelis paeta.J. Henan Agric. Sci. 2006,5, 18.
142.
Lü, J.H.; Shi, Y.L. The bioactivitiy of essential oil from Ailanthus altissima Swingle (Sapindales: Simaroubaceae) bark on
Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae). Adv. Mater. Res. 2012,365, 428–432. [CrossRef]
143. Wei, J.; Kang, L. Roles of (Z)-3-hexenol in plant-insect interactions. Plant Signal. Behav. 2011,6, 369–371. [CrossRef] [PubMed]
144.
Flint, H.M.; Salter, S.S.; Walters, S. Caryophyllene: An attractant for the green lacewing. Environ. Entomol.
1979
,8, 1123–1125.
[CrossRef]
145. Goulson, D. The Garden Jungle: Or Gardening to Save the Planet; Random House: New York, NY, USA, 2019; p. 261.
146.
Gu, X.; Fang, C.; Yang, G.; Xie, Y.; Nong, X.; Zhu, J.; Wang, S.; Peng, X.; Yan, Q. Acaricidal properties of an Ailanthus altissima bark
extract against Psoroptes cuniculi and Sarcoptes scabiei var. cuniculi in vitro. Exp. Appl. Acarol. 2014,62, 225–232. [CrossRef]
147.
Caboni, P.; Ntalli, N.G.; Aissani, N.; Cavoski, I.; Angioni, A. Nematicidal activity of (E, E)-2, 4-decadienal and (E)-2-decenal from
Ailanthus altissima against Meloidogyne javanica. J. Agric. Food Chem. 2012,60, 1146–1151. [CrossRef] [PubMed]
148.
Lucchetti, L.; Zitti, S.; Taffetani, F. Ethnobotanical uses in the Ancona district (Marche region, Central Italy). J. Ethnobiol. Ethnomed.
2019,15, 9. [CrossRef]
149.
Wagner, R.L.; Card, J.A. Ailanthus altissima aqueous extract deters Spodoptera frugiperda oviposition. Gt. Lakes Entomol.
2020
,53, 11.
Available online: https://scholar.valpo.edu/tgle/vol53/iss1/11 (accessed on 25 July 2022).
150.
Wagner, L.R.; Leach, E.M.; Wallace, J.R. Leaf Extract from Ailanthus altissima negatively impacts life history aspects in
Spodoptera frugiperda (Lepidoptera: Noctuidae). J. Kansas Entomol. Soc. 2021,93, 140–152. [CrossRef]

Diversity 2022,14, 680 16 of 16
151.
Souza, J.R.; Carvalho, G.A.; Moura, A.P.; Couto, M.H.; Maia, J.B. Impact of insecticides used to control Spodoptera frugiperda (JE
Smith) in corn on survival, sex ratio, and reproduction of Trichogramma pretiosum Riley offspring. Chil. J. Agric. Res.
2013
,73,
122–127. [CrossRef]
152.
Lu, J.-H.L.; Lu, Y.J.; Tan, Y.B.; Liu, J.J.; Zhong, J.F. The controlling effects of plant extracts on Oryzaephilus surinamensis (Linnaeus).
J. Henan Uni. Tech. 2006,3, 17–20.
153.
Chermenskaya, T.D.; Stepanycheva, E.A.; Shchenikova, A.V.; Chakaeva, A.S. Insectoacaricidal and deterrent activities of extracts
of Kyrgyzstan plants against three agricultural pests. Ind. Crops Prod. 2010,32, 157–163. [CrossRef]
154.
Stepanycheva, E.A.; Chermenskya, T.D.; Chakaeva, A.S. Effect of biologically active substances of Ailanthus altissima Mill.
Swingle)(Simarubaceae) on spider mite Tetranychus urticae Koch (Akari: Tetranychidae). Agric. Chem.
2011
,4, 52–59. (In Russian)
155.
Polonsky, J.; Bhatnagar, S.C.; Griffiths, D.C.; Pickett, J.A.; Woodcock, C.M. Activity of quassinoids as antifeedants against aphids.
J. Chem. Ecol. 1989,15, 993–998. [CrossRef]
156.
Pavela, R.; Zabka, M.; Tylova, T.; Kresinova, Z. Insecticidal activity of compounds from Ailanthus altissima against
Spodoptera littoralis
larvae. Pak. J. Agric. Sci.
2014
,51, 101–112. Available online: https://pakjas.com.pk/papers/2248.pdf
(accessed on 25 July 2022).
157.
Fokt, H.; Pereira, A.; Ferreira, A.M.; Cunha, A.; Aguiar, C. How do bees prevent hive infections? The antimicrobial properties of
propolis. Curr. Res. Technol. Educ. Top. Appl. Microbiol. Microb. Biotechnol. 2010,1, 481–493.
158. Connolly, J.D.; Hill, R.A. Triterpenoids. Nat. Prod. Rep. 2011,28, 1087–1117. [CrossRef]
159.
Slave, J. Effects of Calcium hydroxide and Quassia extract on Honey bees (Apis mellifera). In Proceedings of the 18th International
Conference on Organic Fruit-Growing, Hohenheim, Germany, 19–21 February 2018; Foerdergemeinschaft Oekologischer Obstbau
e.V. (FOEKO): Weinsberg, Germany, 2018; pp. 247–248.
160.
Yang, K.; Wen, X.; Ren, Y.; Wen, J. Control of Eucryptorrhynchus scrobiculatus (Coleoptera: Cuculionidae), a major pest of
Ailanthus altissima
(Sapindales: Simaroubaceae), using a modified square trap net. J. Econ. Entomol.
2018
,111, 1760–1767.
[CrossRef]
161.
Todorova, T.; Boyadzhiev, K.; Shkondrov, A.; Parvanova, P.; Dimitrova, M.; Ionkova, I.; Kozuharova, E.; Chankova, S. Screening
of Amorpha fruticosa and Ailanthus altissima extracts for genotoxicity/antigenotoxicity, mutagenicity/antimutagenicity and
carcinogenicity/anticarcinogenicity. BioRisk 2022,17, 201–212. [CrossRef]